Reactive Fe(III) minerals can influence methane (CH4) emissions by inhibiting microbial methanogenesis or by stimulating anaerobic CH4 oxidation. The balance between Fe(III) reduction, methanogenesis, and CH4oxidation in ferruginous Archean and Paleoproterozoic oceans would have controlled CH4 fluxes to the atmosphere, thereby regulating the capacity for CH4 to warm the early Earth under the Faint Young Sun. We studied CH4 and Fe cycling in anoxic incubations of ferruginous sediment from the ancient ocean analogue Lake Matano, Indonesia, over three successive transfers (500 days in total). Iron reduction, methanogenesis, CH4 oxidation, and microbial taxonomy were monitored in treatments amended with ferrihydrite or goethite. After three dilutions, Fe(III) reduction persisted only in bottles with ferrihydrite. Enhanced CH4 production was observed in the presence of goethite, highlighting the potential for reactive Fe(III) oxides to inhibit methanogenesis. Supplementing the media with hydrogen, nickel and selenium did not stimulate methanogenesis. There was limited evidence for Fe(III)-dependent CH4 oxidation, although some incubations displayed CH4-stimulated Fe(III) reduction. 16S rRNA profiles continuously changed over the course of enrichment, with ultimate dominance of unclassified members of the order Desulfuromonadales in all treatments. Microbial diversity decreased markedly over the course of incubation, with subtle differences between ferrihydrite and goethite amendments. These results suggest that Fe(III) oxide mineralogy and availability of electron donors could have led to spatial separation of Fe(III)-reducing and methanogenic microbial communities in ferruginous marine sediments, potentially explaining the persistence of CH4 as a greenhouse gas throughout the first half of Earth history.
Iron (Fe) and copper (Cu) are essential cofactors for microbial metalloenzymes, but little is known about the metalloenyzme inventory of anaerobic marine microbial communities despite their importance to the nitrogen cycle. We compared dissolved O2, NO3−, NO2−, Fe and Cu concentrations with nucleic acid sequences encoding Fe and Cu-binding proteins in 21 metagenomes and 9 metatranscriptomes from Eastern Tropical North and South Pacific oxygen minimum zones and 7 metagenomes from the Bermuda Atlantic Time-series Station. Dissolved Fe concentrations increased sharply at upper oxic-anoxic transition zones, with the highest Fe:Cu molar ratio (1.8) occurring at the anoxic core of the Eastern Tropical North Pacific oxygen minimum zone and matching the predicted maximum ratio based on data from diverse ocean sites. The relative abundance of genes encoding Fe-binding proteins was negatively correlated with O2, driven by significant increases in genes encoding Fe-proteins involved in dissimilatory nitrogen metabolisms under anoxia. Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content. A comparison of the taxonomy of genes encoding Fe- and Cu-binding vs. bulk proteins in OMZs revealed that Planctomycetes represented a higher percentage of Fe genes while Thaumarchaeota represented a higher percentage of Cu genes, particularly at oxyclines. These results are broadly consistent with higher relative abundance of genes encoding Fe-proteins in the genome of a marine planctomycete vs. higher relative abundance of genes encoding Cu-proteins in the genome of a marine thaumarchaeote. These findings highlight the importance of metalloenzymes for microbial processes in oxygen minimum zones and suggest preferential Cu use in oxic habitats with Cu > Fe vs. preferential Fe use in anoxic niches with Fe > Cu.
The biomass of all living organisms consists of approximately 30 out of 92 naturally occurring elements [1, 2]. Nitrogen and carbon are the only two elements that can be directly incorporated into biomass via microbial fixation of gaseous forms; N2, CO2, CO, CH4 and other hydrocarbons can be fixed into biomass. The remaining ∼28 elements required for life must be acquired from chemical species dissolved in water or in some cases can be solubilized from rocks and minerals. Nutrients by definition are essential elements or vitamins required for incorporation into cellular biomass, which distinguishes them from energy sources involved in cellular ATP generation. Nutrients may limit cellular growth due to low abundance and/or bioavailability. Extreme environments often possess unique chemical compositions due to extreme temperature or pH, producing nutrient-limited conditions. In some instances, nutrient limitation increases microbial sensitivity to other extreme conditions; for example, Deinococcus radiodurans exhibits increased radiation sensitivity when grown under nutrient limitation .
Methane is a product of and substrate for microbial metabolisms in the deep subsurface, but little is known about microbial metabolisms in deep methane hydrate-bearing sediments. We analyzed microbial community diversity and function in subsurface sediments beneath Hydrate Ridge, offshore Oregon (ODP Leg 204 Site 1244). We targeted four geochemically distinct sediment zones: near surface (2 mbsf), sulfate-methane transition zone (4 and 8 mbsf), iron-manganese reduction zone (18 and 20 mbsf) and deep subsurface (35 and 69 mbsf). Reactive iron increased with depth from 2 mbsf (0.4%) to 21 mbsf (1.1%), where dissolved iron and methane concentrations also peaked. The proportion of archaeal sequences decreased with depth, with deeper sediments dominated by Atribacteria and Chloroflexi. There was a resurgence of uncultivated archaeal groups (10% SAGMEG-1 and 16% MBGB) in the iron-manganese reduction zone. Illumina HiSeq metagenomic sequencing of genomic DNA subjected to single cell multiple displacement amplification resulted in 336 million total and 33.7 million coding reads. The taxonomic affiliations of metagenomic sequences corroborated the trend of increasing Atribacteria genes with depth, but a higher percentage of Chloroflexi sequences. ESOM assembly yielded two Atribacteria genomes of ≤5% contaminationfrom 2 vs. 69 mbsf with 55% and 37% completeness, respectively. Genes for amino acid transport and peptide fermentation, as well as Ni-Fe hydrogenases and the Wood-Ljungdahl carbon fixation pathway, were present. This grant entrained two early-career female researchers not previously funded by C-DEBI, and resulted in eight new collaborations and eight research presentations. All data are available at http://www.bco-dmo.org/project/626690.